The risks of fish parasites, especially nematodes, to human
and animal health constitute are an important problems. The
infections are not only caused health deficiency or disability of
humans and animals but also reduce productivity and
profitability of aquacultute, increase economic burden due to
the costs for disease treatment and prevention. Although
parasitic deseases caused many harmfulness, they have received
little attention from scientists, managements.
Our study of the composition of the parasitic nematodes in
marine fishes in the off Vietnam is urgently needed. The
survey’s results are not only provide the information about the
fauna of fish’s nematoda, the relation between hosts-parasites,
but also assess the the potential risks for human consumption.
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MINISTRY OF EDUCATION
AND TRAINING
VIETNAM ACADEMY OF
SCIENCE AND TECHNOLOGY
GRADUATE UNIVERSITY SCIENCE AND TECHNOLOGY
----------------------------
HOANG VAN HIEN
NEMATODE SPECIES COMPONENT
IN SOME PERCIFORMES FISHES
IN COASTAL REGIONS OF VIET NAM
Major: Parasitology
Code: 9 42 01 05
SUMMARY OF BIOLOGY DOCTORAL THESIS
HA NOI - 2019
The thesis is completed at:
GRADUATE UNIVERSITY SCIENCE AND TECHNOLOGY
VIETNAM ACADEMI OF SCIENCE AND TECHNOLOGY
Supervisors:
1: Ass. Prof. Dr. Ha Duy Ngo
2: Dr. Nguyen Van Duc
Reviewer 1: ........................................................................
...........................................................................................
Reviewer 2: ........................................................................
...........................................................................................
Reviewer 3: ........................................................................
...........................................................................................
The dorteral thesis will be defended at the Evaluation Committee of:
GRADUATE UNIVERSITY SCIENCE AND TECHNOLOGY
Time: Date......month.......2019
The thesis can be found at:
- The library of Graduate University Science and Technology
- National Library of Vietnam
1
INTRODUCTION
1. THE THESIS NECESSARY
The risks of fish parasites, especially nematodes, to human
and animal health constitute are an important problems. The
infections are not only caused health deficiency or disability of
humans and animals but also reduce productivity and
profitability of aquacultute, increase economic burden due to
the costs for disease treatment and prevention. Although
parasitic deseases caused many harmfulness, they have received
little attention from scientists, managements.
Our study of the composition of the parasitic nematodes in
marine fishes in the off Vietnam is urgently needed. The
survey’s results are not only provide the information about the
fauna of fish’s nematoda, the relation between hosts-parasites,
but also assess the the potential risks for human consumption.
2. OBJECTIVES
To have the knowleadge of the nematode fauna from
Perciformes fishes in the sea off Vietnam.
3. THE RESEARCH CONTENTS
* To study and build the systematic of nematode fauna from
Perciformes fishes in the off Vietnam.
* To describe the morphological features of some selected
nematode species.
* To know the current status of nematode infections
(prevalence, intensity of infection) in some Perciformes fish
species (Perciformes) in the off Vietnam.
2
4. THE SCIENTIFIC AND PRACTICE SIGNIFICANCE
OF THE THESIS
- Providing the composition and the distribution of the
parasitic nematodes from Perciformes fishes in the off
Vietnam,, including a new records of host species. Especially,,
19 nematode species were found and described for the first time
in Vietnam.
- Providing the morphological data (measurement, drawings
and images, classification system) of all nematode species
which were collected in this study.
- Contributing the data of parasitic nematodes for the book
"Fauna of Vietnam: Parasitic roundworm in Vietnamese marine
fishes" later.
5. THE THESIS STRUCTURE
The thesis consists of 150 pages, in which: Introduction
2 pages; Literature review 20 pages; Materials and research
methods 13 pages; Results and Discussions 104 pages;
Conclusion and Suggestions 1 page. The published works,
which are related to the thesis 1 page; References 9 pages,
include 13 documents in Vietnamese and 81 documents in the
foreign languages. The thesis has 11 tables, 47 figures and
illustrations, diagrams and 16 appendix pages.
I. Chapter 1. OVERVIEW
1.1. Basic characters of parasitic nematodes: General
morphological features, biological characters, life cycle of
nematodes, the distribution and harmfull effects of nematodes
were provided.
3
1.2. Summary of the parasitic roundworm classification
system: The outline of the nematode classification system in
the World and Vietnam were summarized.
1.3. Some basic characters of the Vietnamese marine fish
fauna, including the Perciformes order: General characters of
marine fish fauna in Vietnam, especially fishes belong to
Perciformes order were mentioned.
1.4. The studying situation of parasitic nematodes in marine
fishes.
1.4.1. Research on parasitic nematodes in marine fishes in
the Western Pacific region
Research on parasitic helminths in marine animals has been
conducted since the late 19th century, but it was received more
attention by scientists from the miStole of the 20th century.
Particularly, the data of nematode fauna from the Western
Pacific region has been avaiable about three late decades.
Wu (1927) had the first report of parasitic nematode from
marine fish in the off China, the author described one nematode
species Paraleptus scyllii from sharkes Chiloscyllium
plagiosum in Taiwan sea . Up to 1965, Chinese scientists
continued to investigate the parasite fauna from marine fishesin
this region. In 2011, Peng et al. listed a total of 90 species of
nematodes belonging to 31 genera, 13 families, 9
supperfamilies, 3 orders and 2 subclasses in marine fishes in
China. However, this list already included all species (19
nematode spcies) which were found by scientists from Vietnam
and the former Soviet Union in the East Sea of Vietnam (South
China Sea).
4
Arthur et al. (1997) listed 201 parasitic species in Philippine
fishes, including 20 species of nematoda. In this list has
presented of Capillaria philippinensis, which can infecting to
human.
In Thailand, Purivirojkul (2004) found 11 nematode species
from marine fishes.
Jakob et al. (2006) identified 38 helminthic species in
marine fish in Java Island, Indonesia; including 5 nematoda
species.
Akhtar et al. (2006) recorded 7 families, 9 subfamilies, 23
genera and 71 species of nematoda from fishes in the off
Pakistan. Later, Kazmi et al. (2013) listed 90 nematode species
in whole country.
In Japan, studies on parasitic helminths in marine fish were
early carried out, e.g. Layman (1930)found the species
Capillaria helenae. Recently, Nagasawa et al. (2007) identified
7 nematode species of 7 genera.
Arthur et al. (2015) has recorded 24 species of nematode
parasites in fish in the off Malaysia. Almost species were
identified to genus.
1.4.2. The studying situation of parasitic nematode from
marine fishes in Vietnam.
Research on the system of the parasitic helminth from
marine fishes in Vietnam has only been carried out after 1960.
The Russian scientists autopsied 1,118 individuals of 53 fish
species, 16 families from the off East Sea. Among them, 888
individuals of 44 species belong to Perciformes. The authors
5
have discovered and described 42 new species, including one
species of Nematoda.
Le Van Hoa et al. (1972), the first Vietnamese
parasitologists, described 2 new Bulbocephalus species from
Thread finfish.
Hà Duy Ngọ et al. (2009) found 2 nematode species genera
Capillaria and Anisakis in the off Ha Long, Quang Ninh
Province.
Vo The Dung (2010) detected 54 parasitic species from the
grouper Epinephelus spp. in the off Nha Trang, Khanh Hoa
province, including 34 identified species and 20 other
unidentified species. Especially, 8 nematode species were listed.
Nguyen Van Ha (2011) described a new species Ascarophis
moraveci from 3 fish species in the off Ha Long, Quang Ninh
province.
Dang Nguyen Anh Tuan et al. (2015) recorded a species
Camallanus sp. from Parupeneus spp. in off Nha Trang, Khanh
Hoa province.
Chapter 2. MATERIALS AND METHODS
2.1. Subjects, sites and time of the study
2.1.1. Subjects of the study
Subjects of this study were parasitic nematodes that
collected on from Perciformes marine fishes. .
2.1. 2. Time of the study: from 10/2014 to 12/2017
2.1.3. Places of study: Nine provinces of 3 coastal regions in
Vietnam (Figure 1)
6
Figure 1: Study sites
2.2. Study methods
Nematode specimens were collected by using a
“comprehensive examination” method of Skrjabin (1928).
Samples were fixed, and made slides by using a method of De
Grisse (1969). Morphological characters of nematodes were
7
studied by using photographic scanning of electron microscope
(SEM) (Fagerholm , 1982) or by light microscope (Olympus
CH40); all characters were drawings with the aid of camera
lucida and then were redrawn using Adobe Illustrator CS6. All
measurements are also given. Larval samples were examined by
using molecular . All nematode specimens are preserved and
stored at the Department of Parasitology, Institute of Ecology
and Biological Resources.
The references which most using for identification of
nematodes are listed below:
- Systema helminthum, Volume III, part I - The nematodes of
vertebrates (Yamaguti, 1961).
- Keys to the Nematode Parasites of Vertebrates (Anderson et
al., 2009).
- Systematic position and phylogeny. In Lee D. L. (Eds), The
biology of nematodes (De Ley et al., 2002).
- A new system for Nematoda: combining morphological
characters with molecular trees, and translating clades into
ranks and taxa In Nematology Monographs and Perspectives
(De Ley et al., 2004).
- Trichinelloid nematodes parasitic in cold-blooded vertebrates
(Moravec, 2001).
- Metazoan parasites of Salmonid fishes of Europe (Moravec, 2004).
The fish hosts were identified by morphological method,
using the references below: Fauna of Vietnam, episode 17; 19
(Sea bass); FAO species identification guide for fishery
purposes; Database of fishes (www.fishbase.org).
8
Chapter 3. RESULTS
3.1. The composition of parasitic nematodes from Sea bass fishes in the off Vietnam.
A total of 7951 individuals of nematoda, including 2717 adults and 5234 larvae, were collected from
3735 individuals of 129 species, 38 families of the Perciformes in the off Vietnam. Thirdty sevennematode
species belonging to 2 classes, 2 order, 9 families and 21 genera were identified, including, 24 species have
been identified at species level, 13 species have been identified at genus level. Especially, 19 species were
the first time found in Vietnam, and one species Cucullanus(Cucullanus) sp. could be a new species. 26 fish
species are recorded as new hosts for the nematode fauna. The results are shown in Table 3.1:
Table 3.1: Composition of parasitic nematode species in some fish species of the Sea bass in Vietnam
coastal waters
No. Nematoda Host (fishes)
Site
in
host
Prevalence
(%)
Intensity
(Min-
Max)
QN HP NĐ NA QB TTH KH KG BL
PHYLUM NEMATODA POTTS, 1932
Class Enoplea Inglis, 1983
Order Trichinellida Hall, 1916
Familly Capillariidae Railliet, 1915
Genus Capillaria Zeder, 1800
1 Capillaria sp.
Decapterus maruadsi Stomuch 11,43 1-12 x
Seriola dumerili Stomuch 22,73 1-5 x
PHYLUM NEMATODA POTTS, 1932
Class Chromadorea Inglis, 1983
Order Rhabditida Chitwood, 1933
9
Familly Anisakidae Skrjabin & Karokhin, 1945
Genus Anisakis Dujardin, 1845
2
Anisakis typica*
(Diesing, 1860)
Baylis, 1920
Carangoides malabaricus Cavity 4,11 1-5 x
Decapterus macarellus Cavity 19,35 1-9 x
Lutjanus johnii Cavity 4,17 1;3 x
Megalaspis cordyla Cavity 5,88 1-3 x
Priacanthus hamrur Cavity 33,89 1-18 x
Pristipomoides filamentosus Cavity 30 1-2 x
Sargocentron rubrum Cavity 1/8 2 x
Trichiurus lepturus Cavity 16,46 1-5 x x
Genus Contracaecum Railliet & Henry, 1912
3
Contracaecum
osculatum*
(Rudolphi, 1802)
Baylis, 1920
Alectis ciliaris Cavity 5,56 1;2 x x
Atropus atropus Intestin 10,34 3-14 x x
Scomberoides commersonianus Intestin 12 2-7 x
Dentex tumifrons Intestin 50 4-27 x
Lutjanus vitta Intestin 50 1-14 x x x x x
Otolithes ruber Intestin 12,24 2-12 x x
Penhania argentata Cavity 34,48 2-8 x
Rastrelliger brachysoma Cavity 7,41 3-8 x x x
Sarda orientalis Intestin 10 1 x
Selar crumenophthalmus Cavity 17,39 1-14 x x x
Siganus canaliculatus Intestin 5/5 23-100 x
10
Trichiurus lepturus Cavity 27,85 3-24 x x
4 Contracaecum sp.
Acanthopagrus latus Cavity 40 1-12 x
Alepes kleinii Cavity 8,55 1-8 x x x x x
Carangoides hedlandensis Cavity 90 5-52 x
Eleutheronema tetradactylum Cavity 10,20 2-12 x x x
Epinephelus amblycephalus Cavity 19,30 1-6 x x x x x
Epinephelus areolatus Cavity 37,50 1-3 x
Gerres filamentosus Cavity 31,75 5-27 x x
Gerres oyena Cavity 20,34 1-15 x x x
Jhonius belangerii Cavity 5,77 6-31 x x
Larimichthys croceus Cavity 2,86 4 x
Polynemus melanochir Cavity 20 1;9 x
Genus Terranova Leiper & Atkinson, 1914
5 Terranova sp*. Siganus fuscescens Intestin 0,85 2 x
Genus Goezia Zeder, 1800
6 Goezia sp*. Eleutheronema tetradactylum ** Stomuch 6,12 1-5 x
Familly Raphidascarididae Hartwich, 1954
Genus Hysterothylacium Ward & Magath, 1917
7
H. aduncum
Rudolphi, 1802
Alepes kleinii Intestin 7,69 1-7 x x x x x
Carangoides malabaricus Intestin 27,40 1-11 x x x
Cephalopholis miniata Intestin 3/5 1-3 x
Dentex tumifrons Intestin 40 4-30 x
11
Epinephelus retouti Intestin 7,14 1 x
Evynnis cardinalis Intestin 58,06 1-6 x x
Lutjanus russelli Intestin 1,96 5 x
Nemipterus japonicus Intestin 21,21 1-12 x
Otolithes ruber Intestin 8,16 3-7 x x x
Pomadasys maculatus Intestin 1,67 2 x
Priacanthus macracanthus Intestin 20 1-2 x
Sargocentron rubrum Intestin 2/8 3;7 x
Siganus virgatus Intestin 2,86 1 x
Sillago Aeolus Intestin 6,67 2 x
Terapon jarbua Intestin 18,47 1-6 x x x x
8
H. chorinemi
(Parukhin, 1966)
Bruce & Cannon, 1989
Nemipterus hexodon ** Intestin 37,14 4-17 x
Upeneus sulphureus ** Intestin 86,36 1-18 x
Upeneus tragula ** Intestin 14,63 1-23 x
9
H. fabri*
(Rudolphi, 1819)
Deardorff &
Overstreet, 1980
Uranoscopus oligolepis Stomuch 58,82 1-40
x
10
H. longilabrum*
Li, Liu & Zhang, 2012
Siganus fuscescens Intestin 41,53 5-148 x x x x x x x x x
11 Hysterothylacium sp.
Nemipterus marginatus Intestin 6/8 2-24 X
Parupeneus macronemus Intestin 6,67 6 X
Upeneus moluccensis Intestin 26,67 2-7 x
12
Upeneus tragula Intestin 24,39 4-18 x x x x
Genus Raphidascaris Railliet & Henry, 1915
12
Raphidascaris
acus* Bloch, 1779
Acanthocepola limbata Intestin 20 1;2 x
Acanthopagrus berda Intestin 4,11 1-4 x x
Acautrogobius canius Intestin 30,77 1-6 x x
Argyrosomus japonicus Intestin 13,33 1-20 x
Ariomma indicum Intestin 10,53 1;2 x x
Atropus atropus Intestin 20,69 1-12 x x
Bostrychus sinensis Intestin 20 1;4 x
Butis butis Intestin 21,74 2-11 x x
Carangoides malabaricus Intestin 16,44 2-7 x x x x x
Coryphaena hippurus Intestin 1/5 3 x
Dcapterus maruadsi Intestin 48,57 1-128 x x x
Decapterus macarellus Intestin 51,61 1-13 x x
Eubleekeria jonesi Intestin 53,33 4-28 x
Glossogobius giuris Intestin 20 1-7 x x
Leiognathus equulus Intestin 10,14 1-12 x x
Megalaspis cordyla Intestin 1,47 4 x x
Nemipterus bathybius Intestin 46,67 1-21 x x
Nemipterus japonicus Intestin 21,21 2-18 x x
Otolithes ruber Intestin 12,24 2-7 x x
Pampus chinensis Intestin 11,11 2-7 x x
13
Priacanthus macracanthus Intestin 10 2 x
Rastrelliger brachysoma Intestin 12,35 1-8 x x
Selar crumenophthalmus Intestin 13,04 3-23 x x
Sillago sihama Intestin 6,25 1-3 x
Sphyraena jello Intestin 9,43 1-5 x x
13 Raphidascaris sp.
Alepes kleinii Intestin 8,55 1-11 x x x x x
Atule mate Intestin 6,67 4 x
Chorineruus lasaus Intestin 24,53 1-10 x
Diagramma pictum Intestin 10 3;7 x x
Drepane punctate Intestin 11,11 2;3 x
Epinephelus epistictus Intestin 100 2-4 x
Epinephelus fasciatus Intestin 10 3 x x
Gazza minuta Intestin 30 1-4
Gerres limbatus Intestin 5,48 2-13 x x
Leiognathus splendens Intestin 4 5;17 x x
Leiognathus equulus Intestin 5,79 2-17 x x
Lethrinus lentjan Intestin 20 5;12 x
Lutjanus johnii Intestin 8,33 2-7 x
Lutjanus russelli Intestin 3,92 1;3 x
Megalaspis cordyla Intestin 1,47 5 x
Parastromateus niger Intestin 6,67 2-8 x
Platax teira Intestin 33,33 2-8 x
14
Pterocaesio chrysozona Intestin 23,08 1-12 x
Scomberoides commersonianus Intestin 8 2;9 x x
Selaroides leptolepis Intestin 61,90 4-27 x
Trachinotus baillonii Intestin 5 7 x
Genus Raphidascaroides Yamaguti, 1941
14
R. nipponensis*
Yamaguti, 1941
Dactyloptena orientalis
** Intestin 6,67 1
x
Familly Ascarididae Baird, 1853
Genus Porrocaecum Railliet & Henry, 1915
15 Porrocaecum sp. Nimepterus Japonicus ** Intestin 3,03 7-12 x
Familly Quimperiidae (Gendre, 1928) Baylis, 1930
Genus Haplonema Ward & Magath, 1917
16 Haplonema sp*. Terapon jarbua ** Intestin 1,27 1;3 x x
Familly Cystidicolidae Skrjabin, 1946
Genus Ascarophis Van Beneden, 1871
17 Ascarophis sp.
Sargocentron
melanospilos **
Stom 2/8 5;9 x
Epinephelus retouti ** Stom 7,14 1 x
Dentex tumifrons ** Stom 20 2;3 x
18
A. moraveci Ha et
al., 2011
Scatophagus argus Stom 5,80 1-8 x x
Nibea albiflora Stom 22,45 2-17 x x
Genus Spinitectus Fourment, 1883
15
19
S. echenei
Parukhin, 1967
Coryphaena hippurus ** Intestin 3/5 2-9 x
Auxis thazard ** Stomuch 15,52 1-5 x
Genus Prospinitectus Petter, 1979
20
Prospinitectus
mollis (Mamaev,
1968) Petter, 1979
Auxis thazard Stomuch 10,34 2-5
x x
Familly Philometridae Baylis & Daubney, 1926
Genus Buckleyella Rasheed, 1963
21
B. buckleyi
Rasheed, 1963
Jhonius carouna** Intestin 6 1-7
x
Genus Philometra Costa, 1845
22
P. scieanae*
Yamaguti, 1941
Pennahia argentata Intestin 10,34 1-5 x
Priacanthus hamrur ** Intestin 15,25 1-28 x
Genus Philometroides Yamaguti, 1935
23
P. atropi
(Parukhin, 1966)
Moravec &
Ergens, 1970
Scomberoides
commersonianus **
Intestin 4 1
x
Familly Camallanidae Railliet et Henry, 1915
Genus Camallanus Railliet & Henry, 1915
24
Camallanus
carangis Olsen,
1954
Carangoides malabaricus Intestin 5,48 4-9 x
Atule mate ** Stomuch 13,33 2;5 x
25 Camallanus sp. Jhonius carouna ** Intestin 7 2-5 x
16
Nemipterus hexodon ** Intestin 14,29 1-8 x
Genus Procamallanus Baylis, 1923
26
P. annulatus* Yamaguti,
1955
Siganus guttatus ** Stomuch 11,76 1;1
x
27
P. laeviconchus* Wedl,
1862
Siganus virgatus ** Stomuch 2,86 2
x
Genus Procamallanus Baylis, 1923
Subgenus Procamallanus (Spirocamallanus) Olsen, 1952
28
P. (Spirocamallanus)
spiralis* Baylis,
1923
Leiognathus splendens ** Intestin 8 4-22
x
29
P.(Spirocamallanus)
guttatusi
Andrade-Salas,
Pineda-Lopez et
Garcia-Magana, 1994
Lateolabrax japonicus ** Intestin 16 3-8
x
Epinephelus retouti ** Intestin 7,14 7
x
30
P.( Spirocamallanus)
pereirai*
Annereaux, 1946
Otolithes ruber Intestin 4,08 1-15 x
31
P.( Spirocamallanus)
dussumieri*
Bilqees, Khanum
& Jehan, 1971
Jhonius carouna ** Intestin 6 1-8 x x
32 P.(Spirocamallanus) sp.*
Cephalopholis miniata Intestin 2/5 2;4 x
Lethrinus miniatus Intestin 18,18 3;3 x
17
Familly Cucullanidae Cobbold, 1864
Genus Cucullanus Muller, 1777
33
C.heterochrous
Rudolphi, 1802
Scatophagus argus ** Stomuch 10,14 3-21 x
34
C.rastrelligeri*
Thanapon Y., Moravec
F., Chalobol W., 2011
Pomadasys maculatus ** Intestin 1,67 3 x
Sargocentron melanospilos ** Intestin 3/8 1-37 x
Sargocentron rubrum ** Intestin 1/8 4 x
Siganus fuscescens ** Intestin 3,39 1-11 x
35
Cucullanus
(Truttaedacnitis)
Truttae* Fabricius, 1794
Nibea albiflora ** Intestin 24,49 2-13
x x
36
Cucullanus
(Cucullanus)*** sp.
Jhonius carouna Intestin 10 2-14
x x
Genus Dichelyne Jagerskiold, 1902
37 Dichelyne sp. Jhonius belangerii ** Intestin 11,54 3-12 x
Note: * Nematode species was the first recorded in V